Journal of Helminthology (2017) 91, 578–582 doi:10.1017/S0022149X16000754 © Cambridge University Press 2016 Nematode infection patterns in a Neotropical lizard species from an insular mountain habitat in Brazil A.B.H.P. Václav1,3, L.A. Anjos2, M.S. Queiróz2, L.B. Nascimento3 and C.A.B. Galdino3* 1PET Biologia PUC Minas – MEC/SESu, Pontifícia Universidade Católica de Minas Gerais, 30535-901, Belo Horizonte, Brazil: 2Departamento de Biologia e Zootecnia, Laboratório de Parasitologia e Zoologia, UNESP, Universidade Estadual Paulista, FEIS, Passeio Monção 226, CEP 15385-000, Ilha Solteira, Brazil: 3Programa de Pós-graduação em Biologia de Vertebrados, Pontifícia Universidade Católica de Minas Gerais, 30535-610, Belo Horizonte, Brazil (Received 12 July 2016; Accepted 27 September 2016; First published online 28 October 2016) Abstract Neotropical lizards are known to harbour rich nematode parasite faunas; how- ever, knowledge of the diversity and patterns of infection are still lacking for many species. This is true for the genus Tropidurus, in which data on patterns of parasitism are known for only approximately 11 of its 30 species. We show that the nematode fauna associated with a population of Tropidurus montanus is composed of three species of host-generalist parasites with high overall preva- lence. Male and female lizards did not differ in infection pattern and there was no relationship between host body size and intensity of infection for the most prevalent parasite species. Nevertheless, overall prevalence changed seasonally, with a higher proportion of parasitized individuals being found in the dry period than in the rainy period. We discuss our findings in the context of diet patterns of T. montanus, which we suggest may explain the similarities in prevalence and in- tensity of infection between the sexes. In addition, seasonal changes in diet are considered to be related to the observed differences in prevalence between dry and rainy periods. Introduction variation in rainfall, which can, in turn, result in seasonal patterns of infection. Lizards are ectotherms, thus adjusting The major climatic factor influencing ecological systems their activity patterns and behaviours according to environ- in the Neotropics is seasonal variation between dry and mental conditions (e.g. Hatano et al., 2001;Filogonioet al., rainy periods. Changes in the amount of rain and in dur- 2010), and so patterns of helminth infection can be expected ation of the rainy period can affect patterns of infection to vary seasonally as well, reflecting the behavioural adjust- spread and persistence (see Altizer et al., 2006). Therefore, ments of these hosts (Ribas et al., 1995; Vrcibradic et al., parasitic interactions involving Neotropical species are ex- 1999; Pereira et al., 2012;Britoet al., 2014). pected to change over time in response to periodic Lizards are important components of the life cycle of many species of helminths, serving as definitive or inter- mediate hosts (e.g. Ávila & Silva, 2010). The helminth *E-mail: [email protected] fauna that parasitizes lizards is diverse and with varied All authors consented to participation in the study and agreed patterns of infection. In this sense, helminth richness can upon the content of the article. vary geographically among populations (Brito et al., Downloaded from https://www.cambridge.org/core. UNESP-Universidade Estadual Paulista, on 29 May 2019 at 17:00:45, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0022149X16000754 Nematode infection patterns in a Neotropical lizard 579 2014; Galdino et al., 2014), and changes in the composition Post-mortem examinations of the body cavity, digestive of component communities can be unrelated to geograph- tract, liver and lungs were undertaken using a stereomicro- ical distance among populations (Bezerra et al., 2016). scope. Nematodes were cleared with Aman’slactophenol Additionally, some studies have shown divergent results (Andrade, 2000) and analysed using a computerized sys- when considering whether infection rates and parasite tem for image analysis LAS 5.0 (Leica Application Suite), loads of helminths vary between sexes, or whether para- adapted to a DM 2500-Leica microscope with a differential site load is related to host body size. Hence, information interference contrast system (Leica, Wetzlar, Germany). All is still needed for a more complete understanding of the the parasitological terms used followed Bush et al.(1997). epidemiological and ecological patterns of helminth infec- Worms were deposited in the helminthological collection tion in lizards. of the Instituto de Biociências de Botucatu, Universidade The genus Tropidurus is speciose, with 30 species (Uetz Estadual Paulista (species batches: CHIBB 7861; CHIBB &Hošek, 2016). The genus harbours a rich helminth fauna 7862; CHIBB 7863), Botucatu, Brazil. with nearly 30 different parasite species and with compo- Differences between the sexes in overall helminth nent communities hosting from 3 to 21 species (Ávila & prevalence were tested by using the binomial test for Silva, 2010; Anjos et al., 2012). Recently, there have been each of the periods (rainy and dry). The binomial test efforts to uncover the diversity and patterns of helminth was also used to test for differences in prevalence between infection of species of Tropidurus (e.g. Tropidurus itambere, the two periods, considering all individuals in a period re- Ávila et al., 2011; T. hygomi and T. psammonastes, Lambertz gardless of sex. To evaluate the effects of period (dry and et al., 2012; T. spinulosus, Lunaschi et al., 2012; T. torquatus, rainy) and sex on the overall intensity of helminth infec- Pereira et al., 2012; T. oreadicus, Santos et al., 2013; tion we used a two-way analysis of variance (ANOVA). T. hispidus and T. semitaeniatus, Brito et al., 2014); however, Effects of body size on intensity of infection were evalu- parasitological data are missing for approximately 60% of ated for the helminth species with higher prevalence by the species of the genus. conducting a Generalized Linear Mixed Models analysis The occurrence of the lizard T. montanus is restricted to considering each individual as a random effect variable. the rocky outcrop formations of the mountaintop habitats In addition, we used a one-factor permutation test to of the Serra do Espinhaço (Espinhaço mountain range) in evaluate the effect of period on infection intensity of the South America (Rodrigues, 1987). To the best of our more prevalent helminth species (Hothorn et al., 2008). knowledge, information on parasitism of this species by helminths is lacking. The aim of the present study was to describe the helminth species composition and infec- Results tion levels in the Neotropical lizard T. montanus, relative to seasonality, host sex and size. The helminth component community of T. montanus (n = 80) was found to be composed of three species: Parapharyngodon alvarengai Freitas, 1957 (Pharyngodoni- Materials and methods dae) (prevalence = 59%; mean intensity of infection = 5.6 ± 5.1), found in both large and small intestines; Physaloptera We conducted the study in the rocky outcrop formation sp. Rudolphi, 1819 (Physalopteridae) (prevalence = 12%; at c.1460 m above mean sea level in the Serra da Piedade mean intensity of infection = 4.9 ± 8.2), found in the larval (Piedade mountain range; 19°49′S; 43°40′W), a branch of stage in the stomach and large intestine, and Strongyluris the Espinhaço Range, in the state of Minas Gerais, oscari Travassos, 1923 (Heterakidae) (prevalence = 44%; Brazil. High-elevation open habitats of the mountains mean intensity of infection = 6.0 ± 7.2) found in lungs, from eastern Brazil (which include the Espinhaço Range large and small intestines. Therefore, P. alvarengai and and related branches) are considered as isolated insular S. oscari were the most prevalent nematodes found para- environments that play a role in biogeographical sitizing individual lizards. Of the total of 80 lizards processes of plant and animal species (Chaves et al., sampled, 64 were parasitized by at least one species, re- 2015, Neves et al., 2016). The mean annual temperature sulting in an overall prevalence of 80%. Regarding infra- is 21°C and the mean annual rainfall averages 1650 mm. communities, 64% of lizards were parasitized by a The region experiences a marked distinction between single parasite species, while 30% of the hosts were para- rainy (from October to March) and dry (from April to sitized by two and 6% by three species. Nematode September) periods (Alvares et al., 2014). abundance averaged 7.4 ± 6.3. The intensities of infection Sampling of lizards took place during the rainy by P. alvarengai and by S. oscari were not related to host (December 2012) and dry months (June to August 2013). body size (P = 0.07, n = 52 and P = 0.60, n = 50, Lizards were sampled by performing visual encounter respectively). surveys throughout the period of activity of the species, We sampled 17 males and 20 females of T. montanus in and captured by noose or by shooting rubber bands. the rainy period and 21 males and 22 females in the dry Captured lizards were killed by lethal injection of sodium period. In the dry period, 95% of males and 100% of fe- thiopental, measured for body size (snout-to-vent length) males were found to harbour helminths, with no differ- with a Vernier caliper (nearest 0.1 mm), fixed and pre- ence in overall prevalence between the sexes (P = 0.98). served following standard procedures, and deposited in During the rainy period, 70% of males and 50% of females the herpetological collection of the Museu de Ciências were found to be parasitized and there was no difference Naturais of Pontifícia Universidade Católica de Minas in prevalence between males and females for the rainy Gerais (MCNR 4893–4934; 5114–5145; 5159–5174), Belo period (P = 0.34). The population of T. montanus had high- Horizonte, Brazil. er overall prevalence during the dry period (97%) than Downloaded from https://www.cambridge.org/core.